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Genomic Variation in Helianthus: Learning from the Past and Looking to the Future Michael B

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Genomic Variation in Helianthus: Learning from the Past and Looking to the Future Michael B BRIEFINGS IN FUNCTIONAL GENOMICS. VOL 13. NO 4. 328 ^340 doi:10.1093/bfgp/elu004 Genomic variation in Helianthus: learning from the past and looking to the future Michael B. Kantar, Gregory J. Baute, Dan G. Bock and Loren H. Rieseberg Advance Access publication date 3 March 2014 Abstract Helianthus is an economically important and genetically diverse genus, containing both evolutionary model species and cultivated species. Genetic variation within this genus has been examined at many different scales, from genome size changes to chromosomal structure to nucleotide variation. The growing amount of genomic resources within the genus has yielded insights into the importance of paleopolyploid events, and how transposable elements can cause rapid genome size increases. The rapidly evolving chromosomes in Helianthus have provided a system whereby it has been possible to study how chromosomal rearrangements impact speciation, adaptation and intro- gression. Population and quantitative genetic studies have used the abundant nucleotide variation to identify a number of candidate genes which may be involved in both local adaptation and domestication. The results from these investigations have provided basic knowledge about evolution and how to utilize genetic resources for both agriculture and conservation. Targeting Helianthus for further study as new technologies emerge will allow for a better understanding of how different types of genomic variation interact and contribute to phenotypic variation in a complex system that is ecologically and economically significant. Keywords: transposableelements;karyotype;nucleotidevariation;hybridization;speciation INTRODUCTION karyotyping methods and high-throughput DNA Genetic variation is the raw material that natural and sequencing, it is now possible to assess genome- artificial selection acts on. Characterizing the nature wide levels of genetic variation in almost any taxo- and extent of this variation, as well as how it is linked nomic group of interest [5–7]. to phenotypic and ecological diversity has important Helianthus is an exemplar genus for the study implications for evolutionary biology, biodiversity of genetic variation in the wild. Wild sunflowers conservation and plant breeding [1–3]. Until recently occupy a wide variety of habitats, which range the full depth of genetic variation, which spans from from open plains to sand dunes and salt marshes gene and genome duplication to large structural [8]. Native to North America, Helianthus comprises rearrangements and to single nucleotide variation, 12 annual and 37 perennial species [9–11] that have was only being characterized in a limited number been the subject of a number of intensive evolution- of model species (e.g. Arabidopsis thaliana; reviewed ary genetic studies. Within many of these species in [4]). Recent advances in technology, primarily there is ecological and genetic diversification. sequencing technologies, have allowed researchers Motivated in part by the observation that hybridiza- to significantly broaden the taxonomic scope of tion happens rampantly among Helianthus taxa, these efforts. By integrating mapping approaches, this group has been used to dissect the genetic Corresponding author. M.B. Kantar, Department of Agronomy and Plant Genetics, University of Minnesota, 411 Borlaug Hall, 1991 Upper Buford Circle, St. Paul, MN 55108, USA. Tel.: þ1 612 910 3865; Fax: þ1 612 625 1268; E-mail: [email protected] Michael B. Kantar is a post-doctoral scholar at the University of Minnesota’s Department of Agronomy and Plant Genetics and the University of British Columbia’s Biodiversity Research Centre and Department of Botany. Gregory J. Baute is a PhD candidate in the Biodiversity Research Centre and Department of Botany, University of British Columbia. Dan G. Bock is a PhD candidate in the Biodiversity Research Centre and Department of Botany, University of British Columbia. Loren H. Rieseberg is a professor at the Biodiversity Research Centre and Department of Botany, University of British Columbia and Indiana University’s Department of Biology. ß The Author 2014. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected] Downloaded from https://academic.oup.com/bfg/article-abstract/13/4/328/282684 by Harvard Library user on 05 August 2018 Genomic variation in Helianthus 329 determinants of species cohesion [12, 13]. Work on duplication, or polyploidization, has been recognized two widespread annual species—Helianthus annuus as an integral part of plant biology for over a century and Helianthus petiolaris—and their three independent [30, 31]. During the past decade, with the explosion homoploid hybrid derivatives—Helianthus deserticola, of large-scale datasets, the study of polyploidization Helianthus paradoxus and Helianthus anomalus—have has seen increased interest (reviewed in [32]). helped clarify the role of chromosomal rearrange- Particularly productive research themes include the ments and ecological divergence in the formation frequency at which polyploidization events have of hybrid taxa [14–16]. Use of various molecular occurred and their role in biological diversification markers with this system has yielded insights into [33, 34], the genomic consequences of polyploidiza- rates of adaptive molecular evolution [17], genetic tion [35, 36] and the genetic basis of adaptation to changes that accompany or facilitate adaptation polyploidy [37, 38]. In contrast, much less is known to extreme environments [18–20] and the contribu- about genome size variation originating from copy tion of introgressive hybridization to local adaptation number differences of TEs (reviewed in [29]). [21, 22]. Patterns of TE proliferation and deletion have The genus contains two economically important been investigated in a number of systems [39–42]. crops, the annual oilseed crop common sunflower However, the factors responsible for generating these (H. annuus) and the perennial tuber crop Jerusalem patterns remain enigmatic. Here, we provide a synop- artichoke (Helianthustuberosus). Helianthusannuus is the sis of research on genome size variation in Helianthus, more widely grown, being cultivated on 26 mil- with an emphasis on TE dynamics. We provide ex- lion hectares worldwide in 2011 [23]. Grown for its amples of how sunflower research has advanced our edible oil, H. annuus is favored among producers for understanding of this active area of study. its abiotic stress tolerance [24]. Cultivated H. annuus Similarly to the rest of the plant kingdom, has the second largest hybrid seed market in the Helianthus exhibits considerable variation in genome world with a substantial private investment in breed- size (Table 1). Much of this variation is attribut- ing efforts. Genetic analyses performed primarily on able to differences between ploidy levels. Indeed, H. annuus, a species that exhibits a classic domestica- Helianthus contains diploid (2n ¼ 2x ¼ 34), tetraploid tion syndrome, have shed light on genome-wide (2n ¼ 4x ¼ 68) and hexaploid species (2n ¼ 6x ¼ 102) consequences of domestication [25, 26], and have [8, 43] that formed during neopolyploidization facilitated the identification and functional validation events occurring since the radiation of the genus of causal domestication genes [27, 28]. (i.e. 1.7–8.2 million years ago; [44]). Investigations Here, we give an overview of research into using expressed sequence tag data have revealed that genetic variation in the genus Helianthus. We provide all Helianthus species have also undergone at least two examples of how our knowledge of fundamental rounds of older polyploidization events: one at the questions in evolution and genome organization base of the tribe Heliantheae, dated at 26–31 million has been improved by the study of variation in years ago and one at the base of the family genome size, chromosomal structure and nucleotide Compositae, dated at 40–45 million years ago [33]. sequence in wild and domesticated sunflower spe- Beyond identifying a source of genomic redundancy cies. We conclude by highlighting new research in the sunflower genome, these findings revealed opportunities for genetic work in the genus. that retention of duplicated genes is paralleled across different tribes in the Compositae [33], despite 33–38 million years of divergence [45]. The cate- THE DYNAMICS OF GENOME gories of paleologs retained were, however, unlike EXPANSION AND CONTRACTION those recovered in other plant families [46, 47] IN HELIANTHUS (structural components and cellular organization in It has long been known that genome size varies tre- Compositae versus transcription and signaling in mendously across plant species [29]. Duplication of other families [33]), suggesting that forces determin- DNA, both at large scales involving whole genomes ing the fate of duplicates after whole-genome dupli- and chromosomes and small scales where transposable cation, although conserved within lineages, diverge elements (TEs) proliferate, is ultimately responsible at higher taxonomic levels [33]. for genome size increases. The multiplication of Much of the research on genome size variation in whole chromosome sets, known as whole genome Helianthus has been directed toward understanding Downloaded from https://academic.oup.com/bfg/article-abstract/13/4/328/282684 by Harvard Library user on 05 August 2018 330 Kantar et al. Ta b l e 1: Species, ploidy, chromosome number and genome size of all the species in Helianthus for which genome sizes are
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